Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans

Katrin Besser; Graham P Malyon; William Scott Eborall; Giovanni Paro da Cunha; Jefferson Goncalves Filgueiras; Adam Dowle; Lourdes Cruz Garcia; Samuel J. Page; Ray Dupree; Marcelo Fernando Kern; Leonardo Dario Gomez; Yi Li; Luisa Elias; Federico Sabbadin; Shaza E. Mohamad; Giovanna Pesante; Clare G. Steele-King; Eduardo Ribeiro de Azevedo; Igor Polikarpov; Paul Dupree; Simon M. Cragg; Neil Charles Bruce; Simon John McQueen Mason

doi:10.1038/s41467-018-07575-2

Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans

Katrin Besser, Graham P Malyon, William Scott Eborall, Giovanni Paro da Cunha, Jefferson Goncalves Filgueiras, Adam Dowle, Lourdes Cruz Garcia, Samuel J. Page, Ray Dupree, Marcelo Fernando Kern, Leonardo Dario Gomez, Yi Li, Luisa Elias, Federico Sabbadin, Shaza E. Mohamad, Giovanna Pesante, Clare G. Steele-King, Eduardo Ribeiro de Azevedo, Igor Polikarpov, Paul DupreeSimon M. Cragg, Neil Charles Bruce, Simon John McQueen Mason

Research output: Contribution to journal › Article › peer-review

Abstract

Woody (lignocellulosic) plant biomass is an abundant renewable feedstock, rich in polysaccharides that are bound into an insoluble fiber composite with lignin. Marine crustacean woodborers of the genus Limnoria are among the few animals that can survive on a diet of this recalcitrant material without relying on gut resident microbiota. Analysis of fecal pellets revealed that Limnoria targets hexose-containing polysaccharides (mainly cellulose, and also glucomannans), corresponding with the abundance of cellulases in their digestive system, but xylans and lignin are largely unconsumed. We show that the limnoriid respiratory protein, hemocyanin, is abundant in the hindgut where wood is digested, that incubation of wood with hemocyanin markedly enhances its digestibility by cellulases, and that it modifies lignin. We propose that this activity of hemocyanins is instrumental to the ability of Limnoria to feed on wood in the absence of gut symbionts. These findings may hold potential for innovations in lignocellulose biorefining.

Original language	English
Article number	5125
Number of pages	14
Journal	Nature Communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-018-07575-2
Publication status	Published - 3 Dec 2018

Bibliographical note

Keywords

Animals
Cellulose/metabolism
Diet
Digestion/physiology
Feces/chemistry
Gastrointestinal Tract/metabolism
Hemocyanins/metabolism
Isopoda/metabolism
Lignin/metabolism
Microscopy, Electron, Scanning
Microscopy, Electron, Transmission
Wood/parasitology
Xylans/metabolism

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10.1038/s41467-018-07575-2

s41467-018-07575-2
© The Author(s) 2018
Final published version, 2.09 MBLicence: CC BY

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Besser, K., Malyon, G. P., Eborall, W. S., Paro da Cunha, G., Goncalves Filgueiras, J., Dowle, A., Cruz Garcia, L., Page, S. J., Dupree, R., Kern, M. F., Gomez, L. D., Li, Y., Elias, L., Sabbadin, F., Mohamad, S. E., Pesante, G., Steele-King, C. G., Ribeiro de Azevedo, E., Polikarpov, I., ... McQueen Mason, S. J. (2018). Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans. Nature Communications, 9(1), Article 5125. https://doi.org/10.1038/s41467-018-07575-2

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title = "Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans",

abstract = "Woody (lignocellulosic) plant biomass is an abundant renewable feedstock, rich in polysaccharides that are bound into an insoluble fiber composite with lignin. Marine crustacean woodborers of the genus Limnoria are among the few animals that can survive on a diet of this recalcitrant material without relying on gut resident microbiota. Analysis of fecal pellets revealed that Limnoria targets hexose-containing polysaccharides (mainly cellulose, and also glucomannans), corresponding with the abundance of cellulases in their digestive system, but xylans and lignin are largely unconsumed. We show that the limnoriid respiratory protein, hemocyanin, is abundant in the hindgut where wood is digested, that incubation of wood with hemocyanin markedly enhances its digestibility by cellulases, and that it modifies lignin. We propose that this activity of hemocyanins is instrumental to the ability of Limnoria to feed on wood in the absence of gut symbionts. These findings may hold potential for innovations in lignocellulose biorefining. ",

keywords = "Animals, Cellulose/metabolism, Diet, Digestion/physiology, Feces/chemistry, Gastrointestinal Tract/metabolism, Hemocyanins/metabolism, Isopoda/metabolism, Lignin/metabolism, Microscopy, Electron, Scanning, Microscopy, Electron, Transmission, Wood/parasitology, Xylans/metabolism",

author = "Katrin Besser and Malyon, {Graham P} and Eborall, {William Scott} and {Paro da Cunha}, Giovanni and {Goncalves Filgueiras}, Jefferson and Adam Dowle and {Cruz Garcia}, Lourdes and Page, {Samuel J.} and Ray Dupree and Kern, {Marcelo Fernando} and Gomez, {Leonardo Dario} and Yi Li and Luisa Elias and Federico Sabbadin and Mohamad, {Shaza E.} and Giovanna Pesante and Steele-King, {Clare G.} and {Ribeiro de Azevedo}, Eduardo and Igor Polikarpov and Paul Dupree and Cragg, {Simon M.} and Bruce, {Neil Charles} and {McQueen Mason}, {Simon John}",

note = "{\textcopyright} The Author(s) 2018.",

year = "2018",

month = dec,

day = "3",

doi = "10.1038/s41467-018-07575-2",

language = "English",

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Besser, K, Malyon, GP, Eborall, WS, Paro da Cunha, G, Goncalves Filgueiras, J, Dowle, A, Cruz Garcia, L, Page, SJ, Dupree, R, Kern, MF , Gomez, LD , Li, Y, Elias, L, Sabbadin, F, Mohamad, SE, Pesante, G, Steele-King, CG, Ribeiro de Azevedo, E, Polikarpov, I, Dupree, P, Cragg, SM, Bruce, NC & McQueen Mason, SJ 2018, 'Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans', Nature Communications, vol. 9, no. 1, 5125. https://doi.org/10.1038/s41467-018-07575-2

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T1 - Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans

AU - Besser, Katrin

AU - Malyon, Graham P

AU - Eborall, William Scott

AU - Paro da Cunha, Giovanni

AU - Goncalves Filgueiras, Jefferson

AU - Dowle, Adam

AU - Cruz Garcia, Lourdes

AU - Page, Samuel J.

AU - Dupree, Ray

AU - Kern, Marcelo Fernando

AU - Gomez, Leonardo Dario

AU - Li, Yi

AU - Elias, Luisa

AU - Sabbadin, Federico

AU - Mohamad, Shaza E.

AU - Pesante, Giovanna

AU - Steele-King, Clare G.

AU - Ribeiro de Azevedo, Eduardo

AU - Polikarpov, Igor

AU - Dupree, Paul

AU - Cragg, Simon M.

AU - Bruce, Neil Charles

AU - McQueen Mason, Simon John

N1 - © The Author(s) 2018.

PY - 2018/12/3

Y1 - 2018/12/3

N2 - Woody (lignocellulosic) plant biomass is an abundant renewable feedstock, rich in polysaccharides that are bound into an insoluble fiber composite with lignin. Marine crustacean woodborers of the genus Limnoria are among the few animals that can survive on a diet of this recalcitrant material without relying on gut resident microbiota. Analysis of fecal pellets revealed that Limnoria targets hexose-containing polysaccharides (mainly cellulose, and also glucomannans), corresponding with the abundance of cellulases in their digestive system, but xylans and lignin are largely unconsumed. We show that the limnoriid respiratory protein, hemocyanin, is abundant in the hindgut where wood is digested, that incubation of wood with hemocyanin markedly enhances its digestibility by cellulases, and that it modifies lignin. We propose that this activity of hemocyanins is instrumental to the ability of Limnoria to feed on wood in the absence of gut symbionts. These findings may hold potential for innovations in lignocellulose biorefining.

AB - Woody (lignocellulosic) plant biomass is an abundant renewable feedstock, rich in polysaccharides that are bound into an insoluble fiber composite with lignin. Marine crustacean woodborers of the genus Limnoria are among the few animals that can survive on a diet of this recalcitrant material without relying on gut resident microbiota. Analysis of fecal pellets revealed that Limnoria targets hexose-containing polysaccharides (mainly cellulose, and also glucomannans), corresponding with the abundance of cellulases in their digestive system, but xylans and lignin are largely unconsumed. We show that the limnoriid respiratory protein, hemocyanin, is abundant in the hindgut where wood is digested, that incubation of wood with hemocyanin markedly enhances its digestibility by cellulases, and that it modifies lignin. We propose that this activity of hemocyanins is instrumental to the ability of Limnoria to feed on wood in the absence of gut symbionts. These findings may hold potential for innovations in lignocellulose biorefining.

KW - Animals

KW - Cellulose/metabolism

KW - Diet

KW - Digestion/physiology

KW - Feces/chemistry

KW - Gastrointestinal Tract/metabolism

KW - Hemocyanins/metabolism

KW - Isopoda/metabolism

KW - Lignin/metabolism

KW - Microscopy, Electron, Scanning

KW - Microscopy, Electron, Transmission

KW - Wood/parasitology

KW - Xylans/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85057578740&partnerID=8YFLogxK

U2 - 10.1038/s41467-018-07575-2

DO - 10.1038/s41467-018-07575-2

M3 - Article

C2 - 30510200

SN - 2041-1723

VL - 9

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 5125

ER -

Hemocyanin facilitates lignocellulose digestion by wood-boring marine crustaceans

Abstract

Bibliographical note

Keywords

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Leonardo Dario Gomez

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